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TREASURY DEPARTMENT 
UNITED STATES PUBLIC HEALTH SERVICE 

HUGH S. CUMMING, Surgeon General 



ON THE PROBABLE IDENTITY OF THE 

CHITTENDEN-UNDERHILL PELLAGRALIKE SYN 

DROME IN DOGS AND "BLACK-TONGUE" 

WITH REPORT OF NECROPSY FINDINGS 

IN TWO CASES OF BLACK-TONGUE 

BY 

G. A. WHEELER 

Passed Assistant Surgeon 
AND 

JOSEPH GOLDBERGER 

Surgeon, United States Public Health Service 
AND 

M. R. BLACKSTOCK, D. V. S. 
i 

Spartanburg, S. C. 



REPRINT No. 746 

FROM THE 

PUBLIC HEALTH REPORTS 

Mat 5, 1922 
(Pages 1063-1069) 



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1922 



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ON THE PROBABLE IDENTITY OF THE CHITTENDEN-LNDER- 
HILL PELLAGRALIKE SYNDROME IN DOGS AND "BLACK- 
TONGUE." 

WITH REPORT OF NECROPSY FINDINGS IN TWO CASES OF BLACK- 
TONGUE. 1 

By G. A. Wheeler, Passed Assistant Surgeon, and Joseph Goldbeeger, Surgeon, "United State's Public 
Health Service; and M. R. Blackstock, D. V. S., Spartanburg, S. C. 

We desire to invite attention to the striking similarity and probable 
identity of Chittenden and Underbill's pellagralike syndrome in dogs 
and the condition known to American veterinarians as "black- 
tongue." 2 

In August, 1917, Chittenden and Underhill reported the produc- 
tion in dogs of a pathological condition which they regarded as 
closely resembling human pellagra. The condition w T as described as 
follows : 

" The onset of the pathological symptoms is generally very sudden. 
Usually the first abnormal manifestation is a refusal to eat, and ex- 
amination will reveal nothing to account for the loss of appetite. 
The animal lies quietly in its pen and is apathetic. After continued 
refusal to eat for a day or two, the mouth of the dog will present a 
peculiar and characteristic appearance. The inner surface of the 
cheeks and lips and the edges of the tongue are so covered with 
pustules as to give the impression of a mass of rotten flesh. The 
odor from these tissues is foul and almost unbearable. When 
stroked with absorbent cotton the mucous lining of the mouth comes 
away in shreds. Intense salivation is present. The teeth appear to 
be solid and normal. A bloody diarrhea is present, attempts at defe- 
cation being very frequent and resulting in the passage of little 
more than a bloody fluid of foul odor. In some cases, the thorax and 
upper part of the abdomen may contain many pustules half an inch 
in diameter which are filled with pus organisms. No other skin 
lesions are prominent. Death usually results without any particu- 
larly striking features. 

"At autopsy two types of conditions are recognizable: In the ani- 
mals presenting foul mouth and bloody diarrhea the chief interest 
centers in the lower bowel and rectum, which exhibit an intense 
hemorrhagic appearance. With these animals dying rapidly from 
convulsions the only visible abnormality of the alimentary tract is 
the presence in the duodenum of one or more large ulcers." 

This pathological condition was induced by these workers by feed- 
ing a diet of boiled peas, cracker meal, and cottonseed oil. It was 
also induced, but with much greater difficulty, with a diet of meat, 
cracker meal, and lard. 

1 Reprint from ths Public Health Reports, vol. 37, No. 18, May 5, 1922, pp. 1063-1069. 

2 Synonyms: Sore mouth, southern canine plague, dog typhus, dog typhoid, gastroenteritis hemor- 
rhagica, Stuttgart dog epizootic. 

108086—22 1 



2 PELLAGRALIKE DISEASES IN DOGS. 

" Blacktongue " appears to have been first described in 1852 from 
Munich by Hofer as " typhoid of dogs." 3 Hofer mentions among the 
symptoms an abrupt onset, vomiting, retching, and loss of appetite. 
The mucous membrane of the mouth is described as either dirty red 
or yellow, with an evil smelling saliva drooling from the angles of 
the mouth. He remarks that he never observed the typical typhoidal 
stool, but in pernicious cases there was a bloody discharge. At 
necropsy he found congestion of the gastric and intestinal mucosa 
with ulceration scattered throughout the digestive tract. 

Nearly 50 years later, Klett (1899), without knowing of Hofer's 
observation, made a careful and extensive clinical study of the con- 
dition in the course of an outbreak at Stuttgart. A brief summary 
of Klett's clinical observations follows: 

Onset very abrupt with vomiting, followed by loss of appetite and 
by thirst. The dog is indifferent to his surroundings, and his strength 
is diminished. 

The buccal, less often the pharyngeal, mucosa is brownish or dark 
red with erosions and pustules. The mucosa of the tongue is simi- 
larly altered. In advanced cases the mucosa of the mouth, pharynx, 
and tongue becomes covered with a thick chocolate-colored coating. 
The mouth invariably gives off an extremely foul odor. 

Constipation and constipated stools are the rule, but in some cases 
there is uncontrollable diarrhea of a bloody character. 

The conjunctiva is invariably injected. 

The temperature is not above normal. In some cases convulsions 
of a clonic character may occur. 

Other European students have confirmed and, in some details, 
extended Klett's observations, as the result of which it appears that 
some variation in the severity of the disease, but more particularly 
in the prominence or severity of the individual manifestations, may 
occur. Thus the inflammation of the mouth may be slight — it may 
occur without any erosions or ulcerations; on the other hand, it 
appears that the inflammation may be so severe as to lead to de- 
struction (gangrenous) of the anterior part of the tongue. Similarly 
the gastric, duodenal, and rectal mucosa may be but slightly con- 
gested or it may be severely inflamed and ulcerated. 

No extensive study of the disease as it occurs in dogs in the United 
States seems to have been made. There are, however, several pub- 
lished notes describing the salient features of the disease. The fol- 
lowing outline is based on these American accounts and on our own 
observations. 

Onset is rather abrupt, with lassitude, loss of appetite, occasionally 
vomiting, and thirst; the animal, though trying often, may be unable 
to take water. The mouth early gives off a characteristic offensive, 
nauseating odor and soon becomes sore. Salivation develops early, 
and the drooling saliva may become bloody. 

s Hofer's '' Typhus der Hunde" has in the literature been erroneously translated into "dog typhus." 
The German typhus is the English typhoid, and it was typhoid that Hofer meant. 



PELLAGRALIKE DISEASES IN DOGS. 3 

The buccal and lingual mucosa becomes more or less extensively 
injected and inflamed. In some cases .the congestion becomes very 
marked, the mucosa then presenting more or less extensive purplish 
red areas. The tongue,' more particularly the free anterior portion, 
may be thus affected; the margin may be bright red. Both tongue 
and cheeks may become covered with a dirty, gray, slimy coating 
suggestive of a diphtheritic membrane. It is probably this appear- 
ance that led Kerr (1914) to suggest the name "canine diphtheria" 
for the disease. 

The mouth may present erosions and ulcers. Vomiting may 
occur, and either constipation or diarrhea may be present; consti- 
pation is more often a symptom of the onset, diarrhea of the later 
stages. When there is diarrhea the stools may be bloody, particu- 
larly in cases with fatal termination. The temperature may at times 
be considerably elevated. 

The disease appears to end in death in about 75 per cent of cases, 
running its course in these in some four to eight days. 

The American literature on the post-mortem findings is extremely 
meager. The following notes are of two necropsies made by us at 
Spartanburg, S. C, on August 11, 1921. The dogs were Chesapeake 
Bay retrievers, one a male, the other a female, both under 2 years 
of age. One had died 24 hours and the other 10 to 15 hours previously. 

In both animals the lingual and buccal mucosa was found markedly 
but unevenly congested, the congestion involving the mucosa of the 
lips and opposing gums. There was also some congestion of the 
mucosa of the larynx and epiglottis. 

The gastric mucosa showed a patch of moderate congestion in the 
region of the pylorus. 

In one of the dogs there was marked congestion of the mucosa of 
the large gut throughout its whole length, including the rectum; in the 
other no gross change in this part of the bowel was apparent. 

The contents of the gastro-intestinal tract was small in amount; 
in one it was seemingly of a mucous nature, in the other more 
water}^. In both it was yellow-tinged, probably from the medication 
administered just before death. This yellow tinting was also ob- 
served to affect the lingual mucosa and the buccal secretion. 

Examination of the lungs, heart, liver, spleen, and kidneys dis- 
closed no gross lesions. 

The disease has quite generally been regarded as infectious. This 
view seems to be based mainly on its occasional epizootic occurrence 
and in a measure on the observation that at times after the occur- 
rence of one case in a kennel a considerable number, perhaps all, of 
the other dogs are affected. More commonly, however, none of the 
other dogs is attacked, and one finds such observations as the follow- 
ing: "The disease seems to be infectious, and yet I have seen dogs 
drink and eat with the dogs affected with sore mouth and not con- 
tract the disease" (Heiny). "We have five or six dogs of our own 



4 PELEAGRALIKE DISEASES IN DOGS. 

and always have from three to five cases of black tongue at the hos- 
pital, but have never had more than one case of it in our own dogs" 
(Browning) . 

The results of the recorded experimental attempts at transmission 
from sick to well dogs do not lend much support to the conception 
that the disease is an infection, for with one or two doubtful excep- 
tions, these attempts have frankly failed. 

Just as Chittenden and Underbill recognized the resemblance of 
their experimentally induced condition in dogs to pellagra, so there 
have been those who have been struck by the resemblance of the 
naturally occurring disease " black tongue " to the disease in man. 

The first, as far as we have been able to find, to call attention £o 
this is Spencer, of Concord, N. C. In a brief note he states that 
" after studying these two maladies, I am forced to the conclusion 
that the so-called black tongue is canine pellagra and have carried 
on a limited number of experiments to that end." 

Four years later, Cary (1920), of Auburn, Ala., recognizing the 
resemblance of black tongue to the experimental condition reported 
by Chittenden and Underbill, classed "black tongue" among defi- 
ciency diseases and referred to the similarity of the manifestations of 
"sore mouth" in dogs to those of pellagra in man. 

Of interest in this connection is the suggestion by Saunders (1920), 
of Waco, Tex., of some connection between " sore mouth of dogs " and 
pellagra. He writes as follows: "Some five years ago I bought a 
very fine dog in New Jersey and brought him to Texas. The second 
year in Texas he died with what the veterinarian pronounced 'sore 
mouth.' Now, a dog dying with sore mouth was as novel to me as was 
a man dying with pellagra. I noticed that my dog was losing hair 
from his front legs (paws). In commenting on the cause of my dog's 
death with my friends I find that it is a relatively common disease, 
and that there is a large strip of country east of town on a branch 
called the Tehuacana, where they can not have dogs, as they all die 
of the sore mouth. Now, this strip of county has furnished some 
40 or 50 pellagrins to the near-by doctors for treatment. The ques- 
tion is, How much the dog plays in the etiology, or are they both, man 
and dog, infected from the same source, or is the sore mouth a different 
disease and is it a coincidence that they are found here side by side V 

At this juncture it may be remarked that black tongue seems to 
have a geographic distribution in the United States singularly like 
that of pellagra. Seemingly it occurs principally, if not exclusively, 
in the South. Seasonally it is reported to occur most frequently in 
summer and autumn and to affect cur dogs less than those of higher 
grade. There is some evidence that it may occur more than once in 
the same animal. 



PELLAGRALIKE DISEASES IjST DOGS. 5 

The resemblance of black tongue to the experimental condition 
described by Chittenden and Underhill is so striking that it appears 
to us well-nigh certain that the two are identical; but before this 
identity can be accepted as definitely established, much additional 
work will have to be done. The possibility, if not the probability, 
that black tongue in dogs may prove to be the analogue of pellagra 
in man emphasizes the importance of such further investigations. 
In this the individual practitioner can take an important part by 
observing and recording the circumstances of the occurrence of this 
interesting condition in dogs and the efficacy of a strictly dietary 
treatment consisting of milk, eggs, and fresh meat. 

Bibliography. 

The following list includes all original articles on black tongue 
accessible to us. The Italian, literature was not available and is not 
included. Pains were taken to consult and include all possible 
American publications. These have heretofore been pretty generally 
ignored. 

Albrecht: Eine Hundeseuche in Munchen. Thierarztliche Wchnschrift., May 27, 

1899, vol. 7, p. 189. 
Ben-Danon: Sur une affection gastro-intestinale adynamique et athermique chez le 

chien et chez le chat. Rev. Veterinaire, Toulouse, May 1900, vol. 57, p. 293. 
Bimes and Seres: Le typhus de chien (Pasteurellose canine de Lignieres). Rev. 

Veterinaire, Toulouse, Sept. 1, 1901, vol. 58, p. 569. 
Browning: Black tongue in dogs a dietetic disease. Am. Jour. Veterin. Med., 

Chicago, February 1917, vol. 13, p. 113. 
Cary: Deficiency diseases. Jour. Am. Veterin. Med. Assn., March 1920, vol. 66, 

pp. 609-614. 
Chittenden and Underhill: The production in dogs of a pathological condition which 

closely resembles human pellagra. Am. Jour. Physiol., Baltimore, Aug. 1, 1917, 

vol. 44, pp. 13-66. 
Dalrymple: "Foot evil" in horses and mules and "sore mouth" in dogs. Am. 

Veterin. Rev., New York, October 1911, vol. 40, pp. 56-62. 
Davis: Cure for black tongue — maybe. Am. Jour. Veterin. Med., Chicago, March 

1912, p. 116. 

Farmer: Diphtheria antitoxin in black tongue. Am. Jour. Veterin. Med., Chicago, 

1913, vol. 8, p. 332. 

Fisher: Black tongue in dogs an amebic dysentery. Am. Jour. Veterin. Med., 

Chicago, October 1918, vol. 13, p. 515. 
Gundelach: Gastro-enteritis hemorrhagica in verbindung mit stomatitis. Archiv. f. 

Theirheilkunde, Berlin, 1901, vol. 27, p. 308. 
Handley: Southern canine plague. North Am. Veterinarian, Evanston, August 1920, 

vol. 1, pp. 231-234. 
Heiny: Black tongue in Mississippi. Jour. Veter. Med., Chicago, October 1911, 

pp. 790-791. 
Hodges: Black tongue or southern canine plague. North Am. Veterinarian, Evanston, 

November 1921, vol. 2, pp. 556-557. 
Hoerning: Die Stuttgarter Hundeseuche. Inaug. Dissertation, Giessen, Munich, 

1909. 



6 PELLAGRALIKE DISEASES IN DOGS. 

Hofer: Der Typhus der Hunde. Repertorium der Thierheilkunde, Stuttgart, 1852, 

vol. 13, pp. 201-211. 
Hurlimann: Staupenepidemie am Langensee. Schweizer-Arch. f. Thierheilkunde, 

Zurich, 1896, vol. 38, pp. 120-122. 
Kerr: "Black tongue" or "typhus." Am. Jour. Yeterin. Med., Chicago, December 

1914, vol. 9, p. 899. 
Klett: Stuttgarter Hundeseuche. Deutsche Thierarztliche Wchnschrift., Hannover, 

1899, vol. 7, p. 41. 
Klett: The Stuttgart dog epizootic (contagious gastro-enteritis and ulcerative 

stomatitis in the dog). Jour. Compar. Pathol, and Therap., Edinburgh, 1899, 

vol. 13, pp. 36-50. 
Koonce:' Black tongue in dogs. Am. Jour. Yeterin. Med., December 1911, vol. 6, 

pp. 851-854. 
Lucet: Sur la presence de Spirochetes dans un cas de gastro-enterite hemorragique 

chez le chien. Bull, de la soc. Centr. de M6d. Veterinaire, Paris, 1910, vol. 64, 

p. 376. 
Mattel: Die Stuttgarter Hundeseuche. Oesterrechische Monatschrft. f. Thierheil- 
kunde, Wein, 1900, vol. 24, p. 491. 
Mouquet: Contribution a l'etude des suites de typhus "chien." Bull, de la Soc. 

Centrale de Med. Veterinaire, Paris, 1911, vol. 65, p. 134. 
Porter: Black tongue in dogs, etc. Am. Veterin. Rev., New York, December 1911, 

vol. 40, pp. 368-369. 
Quitman: Sodium cacodylate in the treatment of canine typhus. Am. Jour. Veterin. 

Med., Chicago, July 1917, vol. 12, p. 474. 
Rabus: Seuchenartige Erkrankung bei Hunden. Wchnschrft f. Thierheilkunde u. 

Viehzucht, Munich, June 6, 1899, p. 215. 
Richter: Hundeseuche. Berliner Thierarztliche Wchnschrft., Aug. 30, 1900, p. 413. 
Saunders: Pellagra and the "sore mouth of dogs." N. Y. Med. Rec, July 24, 1920, 

vol. 98, pp. 153-154. 
Scheibel: Eine Eigenartige im Herbst 1898 unter den Hunden Frankfurts beobachtete 

Krankheit. Berliner Thierarztliche, Wchnschrft., Feb. 16, 1899, p. 73. 
Spencer: Is "black tongue in dogs pellagra?" Am. Jour. Veterin. Med., Chicago, 

April 1916, vol. 11, p. 325. 
Tremmel: Die Stuttgarter Hundekrankheit in Wien? Thierarztliches Centralblatt, 

Wien, Oct. 1, 1900, vol. 23, p. 453. 
Zschokke: Die Hundeseuche; Gastritis haemorrhagica. Schweizer-Archiv. f. 

Thierheilkunde, Zurich, 1900, vol. 42, p. 241. 

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